Abstract

The human cerebral cortex is a complex network of functionally specialized regions interconnected by axonal fibers, but the organizational principles underlying cortical connectivity remain unknown. Here, we report evidence that one such principle for functional cortical networks involves finding a balance between maximizing communication efficiency and minimizing connection cost, referred to as optimization of network cost-efficiency. We measured spontaneous fluctuations of the blood oxygenation level-dependent signal using functional magnetic resonance imaging in healthy monozygotic (16 pairs) and dizygotic (13 pairs) twins and characterized cost-efficient properties of brain network functional connectivity between 1041 distinct cortical regions. At the global network level, 60% of the interindividual variance in cost-efficiency of cortical functional networks was attributable to additive genetic effects. Regionally, significant genetic effects were observed throughout the cortex in a largely bilateral pattern, including bilateral posterior cingulate and medial prefrontal cortices, dorsolateral prefrontal and superior parietal cortices, and lateral temporal and inferomedial occipital regions. Genetic effects were stronger for cost-efficiency than for other metrics considered, and were more clearly significant in functional networks operating in the 0.09–0.18 Hz frequency interval than at higher or lower frequencies. These findings are consistent with the hypothesis that brain networks evolved to satisfy competitive selection criteria of maximizing efficiency and minimizing cost, and that optimization of network cost-efficiency represents an important principle for the brain's functional organization.

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The key assumption in this interesting paper by Fornito et al. is that a higher correlation among various neuroanatomical parameters in monozygotic twins compared to dizygotic twins can be simply interpreted as evidence for a genetic origin. This may, of course, be true, but it may not be. Monozygotic twins often have a
very different intra-uterine experience than dizygotic twins, and this can, and does, affect their brain d...

The key assumption in this interesting paper by Fornito et al. is that a higher correlation among various neuroanatomical parameters in monozygotic twins compared to dizygotic twins can be simply interpreted as evidence for a genetic origin. This may, of course, be true, but it may not be. Monozygotic twins often have a
very different intra-uterine experience than dizygotic twins, and this can, and does, affect their brain development, and many other features of their later lives.

To take a few of many substantive examples: Loos et al (2001) show that monochorionic monozygotic twins have markedly lower within-pair fibrinogen correlations than dichorionic monozygotic twins; McNeil et al. (2000) analyzed the impact of obstetric complications on the differences in brain anatomy between monozygotic twins; Poulsen and Vaag (2005) show significant differences in
glucose metabolism between all twins and singletons, and between monozygotic twins and dizygotic twins.

There are also methodological difficulties in interpreting twin studies, which are not well considered by Fornito et al. An important paper by Turkheimer et al. (2005) describes the methodological issues in interpreting twin studies with great clarity. Their key point is that it is not possible to show that environmental and genetic influences partition as the SEM models assume, and in fact, that this is an untestable assumption of the models.

A recent NIH workshop (Bookman et al. 2011), published too late for this paper to make use of, outlines some routes towards a fuller understanding of how genes and environment interact to produce health outcomes.

Therefore, the conclusions of Fornito et al. about the genetic component in brain organization may or may not be correct. The authors assume that the traditional simplistic interpretation of complex twin study data is
right, but it may not be, and they have not shown that it is.